A synopsis of knowledge, zoogeography and an online interactive map of Brazilian marine gastrotrichs

Marine ecoregions of the world

We avoided using geopolitical boundaries to analyze gastrotrich distributions because the delimitation of such areas does not reflect natural units (Nihei, 2006). Thus, we used the biogeographic regionalization for coastal and shelf areas proposed by Spalding et al. (2007) to establish the distribution patterns of species. The hierarchical system proposed by these authors has three levels of inclusiveness: ecoregion (smallest-scale unit), province (nested within the realm) and realm (largest spatial unit). In the present study, we used the spatial unit ecoregion, as it is defined as “Areas of relatively homogeneous species composition, clearly distinct from adjacent systems. The species composition is likely to be determined by the predominance of a small number of ecosystems and/or a distinct suite of oceanographic or topographic features” (Spalding et al., 2007).

The system proposed by Spalding et al. (2007) is composed of 232 ecoregions covering all coastal and shelf waters of the world. Among them, five ecoregions occur in Brazil: Amazônia, Northeastern Brazil, Eastern Brazil, Southeastern Brazil and Rio Grande.

The distribution map (Fig. 1) with the known records of Brazilian Gastrotricha species and the worldwide ecoregions was made with the software Quantum GIS (http://www.qgis.org).

Literature database

Distribution data on marine gastrotrichs up to 2010 were obtained from the “Global distribution of marine Gastrotricha” compilation by Dr. William D. Hummon (Todaro, 2017), and from 2011 to 2019, we gathered data directly from the literature (see complete list in Garraffoni & Balsamo, 2017; Todaro et al., 2019) (Fig. 1; Data S1).

Brazilian species records

The species lists of Brazilian gastrotrichs followed the classification proposed by Todaro (2019a, 2019b).

Below the name of each species there is mention about the type locality, a summary of records per country, and the total number of records in Brazil and the world. When possible, a brief remark about the current species distribution and taxonomy status is noted. The list of the geographic coordinates of the locality sites where each species was found are arranged following the world bioregionalization framework of ecoregions (the ecoregions number are the same as those reported by Spalding et al. (2007)), countries and beaches.

Interactive map

All species listed in this paper were entered into a spreadsheet, and an interactive map was produced using My Maps in Google Drive. The map can be accessed at https://www.arcgis.com/apps/View/index.html?appid=4018bc0c77644422a761b8c213eb9c73.

Screenshots from the ArcGis, 2019 Online platform of Marine Gastrotrichs of Brazil are shown in Fig. 2 for instructional purposes. Three views are available: (A) Map view with all records available (B) Map view with only specific species records (C) Map view with image and select data a specific record. Names of species can be displayed using the layer function, where species occurrences can be filtered (Figs. 2A and 2B). Each occurrence in the map is clickable, resulting in a window showing an image of the species and information about the record (Fig. 2C).

Schematic drawings of those species formally described in Brazil were redrawn from original descriptions or redescriptions. Micrographs of Xenodasys sp. were used to exemplify the species collected by researchers from the Laboratory of the Meiofaunal Organisms Evolution and yet not formally described. In this case, samples of the upper sediment layer were collected with a manual corer, and in the laboratory, the specimens were sorted under a stereomicroscope Zeiss DM2000, mounted on glass slides, observed in vivo under a Zeiss Axioskop 2 plus equipped with differential interference contrast and AxioCam MRC5 digital video camera.

Historical study of Brazilian Gastrotricha

This is the first historical review on the gastrotrichs occurring along the Brazilian coast and the first synthesis of the available literature shown as an annotate species checklist. Although the obtained data showed scattered references from Brazilian literature, this panorama has started to change slowly. Historically, in Brazil (and in many other countries of Southern Hemisphere, Hummon, 1974; Hochberg, 2003, 2008; Todaro, Perissinotto & Bownes, 2015; Todaro, Dal Zotto & Leasi, 2015; Todaro et al., 2017), only sporadic collections were carried out by foreign researchers, and the involvement of Brazilian researchers could thus be considered incipient (Balsamo et al., 2014; Garraffoni & Balsamo, 2017). However, a few years ago, the senior author of the present study became the first active native researcher and started to coordinate a research group interested in uncovering the systematics, evolution and biogeography of gastrotrichs. This group has grown over time allowing to start several research projects on these topics.

Garraffoni (2017) noted three major gaps in the current knowledge about Brazilian freshwater Gastrotricha: (a) most of the Brazilian inland waters had never been sampled before. Records, in fact, show a strong bias because most of the samplings were conducted in the State of São Paulo, and only a few in other states); (b) identification keys for a great number of genera do not exist and there is difficulty in obtaining classic and old literature from the end of the century XIX and early century XX; and (c) reference collections about the taxon in Brazilian Museums are absent (see Garraffoni et al., 2019b).

Unfortunately, most of these gaps are also observed for marine animals. Most of the surveys were concentrated on the Northern coast of São Paulo State and the southern coast of Rio de Janeiro State (Todaro & Rocha, 2004, 2005; Todaro, 2012, 2013; Hochberg, 2014; Garraffoni, Di Domenico & Hochberg, 2017; Todaro et al., 2019), and only two studies were performed outside this area (Araújo, Balsamo & Garraffoni, 2014: Bahia State; Araújo et al., 2016: Espírito Santo State) (see below section “Brazilian Gastrotricha distribution patterns”).

The unique Brazilian collection, with adequate and permanent curatorial attention in Brazil, which contains type material regarding marine Gastrotricha is located in the Zoological Museum “Adão José Cardoso” (ZUEC) of the State University of Campinas. This museum houses the type series for Pseudostomella squamalongispinosa Araújo, Balsamo et Garraffoni 2014 (GCH 02-04), Dactylopodola todaroi Garraffoni, Di Domenico et Hochberg, 2016 (GCH 26-28) and Crasiella fonseci Hochberg, 2014. Regarding this last species, due to problems in sending back the type material to Brazil (R. Hochberg, 2018, personal communication), in the original description, it was only mentioned that the holotype was deposited at the ZUEC, but without an accession number. However, we had the possibility to obtain the original type material and deposit it at the ZUEC as GCH-51. Furthermore, additional material was deposited for Pseudostomella dolichopoda Todaro, 2012 (GCH 29). However, the representation of the Gastrotricha physical specimens in Brazilian collections (and also in the world) is extremely poor which is partially reasoned by the gastrotrichs specifies (see Garraffoni et al., 2019b).

The only significant difference between Brazilian marine and freshwater gastrotrichs is related to the number of available identification keys; that mainly exists for marine species. In the last years, taxonomic keys for species belonging to six genera were published, and many listed taxa in Brazil, for example, Aspidiophorus (Todaro et al., 2009); Cephalodasys (Kieneke, Schmidt-Rhaesa & Hochberg, 2015); Dactylopodola (Von Und Zu Gilsa et al., 2014); Paraturbanella (Todaro et al., 2017); Pseudostomella (Clausen, 2004; Todaro, 2012; Araújo et al., 2016) and Tetranchyroderma (Todaro, 2002).

If the taxonomic knowledge of Brazilian gastrotrichs is far from appropriate, also studies on other biological aspects, such as ecology or natural history, are totally absent.

Brazilian Gastrotricha distribution patterns

In general, in recent years, the number of new Gastrotricha species descriptions increased in geographic locations known for poor sampling (Todaro & Rocha, 2004, 2005; Hochberg, 2003, 2008, 2014; Todaro, 2012, 2013; Hochberg, Atherton & Gross, 2013; Von Und Zu Gilsa et al., 2014; Araújo, Balsamo & Garraffoni, 2014; Araújo et al., 2016; Todaro, Leasi & Hochberg, 2014; Todaro, Perissinotto & Bownes, 2015; Todaro, Dal Zotto & Leasi, 2015; Todaro et al., 2017, 2019; Kieneke, Schmidt-Rhaesa & Hochberg, 2015; Garraffoni, Di Domenico & Amaral, 2016; Garraffoni, Di Domenico & Hochberg, 2017; Araújo & Hochberg, 2017; Chatterjee, Priyalakshmi & Todaro, 2019).

In this scenario, when compared the 12 countries of South America, only four (Colombia: Hummon, 1974; Ecuador, Galapagos Island: Schmidt, 1974; and Uruguay: Dioni, 1960) have information available about Gastrotricha fauna, and Brazil can be considered the country with more studies and and descriptions. However, when only Brazil, with a coastline encompassing almost 7,500 km and varying between ~5° and ~25° of longitude, was analyzed, it was found that more than 95% of the country has never been never sampled. However, most of the scientific effort was placed only in the cost of São Paulo State (Todaro & Rocha, 2004, 2005; Todaro, 2012, 2013; Hochberg, 2014; Garraffoni, Di Domenico & Amaral, 2016; Garraffoni, Di Domenico & Hochberg, 2017; Todaro et al., 2019; Supplemental Material 1). It is important to highlight that these results in the State of São Paulo were not accidental but due to many initiatives for funding studies aimed to reveal the biodiversity of fauna and flora in the State that were supported by the Virtual Institute of Biodiversity, BIOTA-FAPESP, organized by FAPESP, the State of São Paulo Research Foundation (Migotto & Tiago, 1999; Joly et al., 2010).

However, if we compared the number of sampled beaches along the São Paulo coastline (26) with the total number of beaches in continental and islands in the State (342), the station coverage is very low, with a very limited number of sampled sites (7% of the total beaches in the state). If considered the states of São Paulo and Rio de Janeiro, which together host 85% of the sampled sites located in Brazil, the sampling site is even worse (4% of the total beaches in both states). For comparison, Italy has a long-standing tradition in the study of Gastrotricha (Balsamo et al., 2014) and the Italian coastline encompasses almost 7,800 km. In this country, gastrotrichs were sampled in 246 localities and comprise 177 different species (Todaro et al., 2003).

As noted above, this difference regarding the knowledge of gastrotrich biodiversity between the Northern and Southern hemispheres occurs because the first studies dedicated to this group of animals were conducted by European or North-American Institutions (Balsamo et al., 2014; Garraffoni & Balsamo, 2017). Unfortunately, many other meiofauna taxa (organisms that pass through 500 μm mesh, but is retained by 44 μm one) present this bias, that is, the distribution of taxon seems to reflect the distribution of specialist more than that of taxon itselves. This bias is commonly known as “rotiferologist” effect (Fontaneto et al., 2012). Thus, this discrepancy in information between the two hemispheres has some consequences; (a) the first record and description of a marine gastrotrichs in the Mediterranean was done by Claparède (1867). In contrast, the first mention of a Brazilian gastrotrich was noted by Eveline du Bois-Raymond Marcus 85 years after the René-Édouard Claparède publication (du Bois-Raymond, 1952), and it was approximately 140 years before Antonio Todaro and Carlos Rocha named the first new species from Brazil (Todaro & Rocha, 2004); (b) 70% of the marine gastrotrich sampling sites around the world are located in the Northern Hemisphere (mainly in Atlantic coast of the United States, German, Poland, Mediterranean and Great Britain coasts) (Garraffoni & Balsamo, 2017); (c) In recent years, the number of studies dealing with the reconstruction of intraphylum relationships of Gastrotricha based on molecular data has increased (Todaro et al., 2011, 2012; Todaro, Leasi & Hochberg, 2014; Todaro, Dal Zotto & Leasi, 2015). However, the DNA used in these studies was mainly extracted from species collected in the Northern Hemisphere.

Despite the bias in sampling sites distribution, the geographic distribution of the Brazilian marine gastrotrichs possesses relatively restricted areas, that is, one or two ecoregions (six species) to widespread distributions, that is, at least four ecoregions (22 species). These numbers have a totally opposite tendency compared to marine gastrotrichs worldwide, as 80% of the species are distributed in only two ecoregions (A.R.S. Garraffoni et al., unpublished data). As a consequence, the absence of wide-scale reviews in the country can produce uncontextualized taxonomic revisions and spurious data on biodiversity. Finally, in recent years, the ubiquitous distribution of marine gastrotrichs has been challenged (Curini-Galletti et al., 2012; Kieneke, Martinez-Arbizu & Fontaneto, 2012; Garraffoni, Di Domenico & Amaral, 2016; Garraffoni & Balsamo, 2017), and the number of widespread species appears not as high as previously thought.

Brazilian Gastrotricha richness

As reported above, due to the low number of taxonomic studies and sample bias along the Brazilian coast, we can provide the estimated richness of gastrotrichs only for the coasts of the states of São Paulo and Rio de Janeiro (Garraffoni, Di Domenico & Amaral, 2016). In this region, besides the 23 formally described species, at least 40 not formally described species were recorded (Todaro & Rocha, 2004, 2005; Garraffoni, Di Domenico & Amaral, 2016; Garraffoni, Di Domenico & Hochberg, 2017): thus, we can say that at least 20 species of marine gastrotrichs from only 5% of the Brazilian coast are waiting to be described. Furthermore, many of these undescribed species belong to very rare taxa, for example, Diplodasys sp., Dolichodasys sp., Mesodasys sp., Paradasys sp., (Todaro & Rocha, 2004), sometimes never reported before from the Southern Hemisphere, for example, Acanthodasys sp1 and sp2 (Garraffoni, Di Domenico & Hochberg, 2017) or Xenodasys sp. collected by the authors of the present study in December 2018 at Fome Beach, Ilhabela Island, Northern coast of São Paulo State (Fig. 3). The last species belongs to a genus with only three species, each with regional (limited) distributions (Schuster et al., 2018).

The large number of unknown species found on the southeastern Brazilian coast is not a surprise. To date, 507 marine gastrotrichs (Garraffoni & Balsamo, 2017; Todaro, 2019a) have been described from all the world’s oceans, but at least 2,244–3,244 species are still unknown and undiscovered (Appeltans et al., 2012). Using species richness as a metric for assessment of the worldwide marine gastrotrich biodiversity, only less than 20% are known (Appeltans et al., 2012).